This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

The authors have chosen to make the review history of this article public.

Abstract

Spiders (Order Araneae) are massively abundant generalist arthropod predators that are found in nearly every ecosystem on the planet and have persisted for over 380 million years. Spiders have long served as evolutionary models for studying complex mating and web spinning behaviors, key innovation and adaptive radiation hypotheses, and have been inspiration for important theories like sexual selection by female choice. Unfortunately, past major attempts to reconstruct spider phylogeny typically employing the “usual suspect” genes have been unable to produce a well-supported phylogenetic framework for the entire order. To further resolve spider evolutionary relationships we have assembled a transcriptome-based data set comprising 70 ingroup spider taxa. Using maximum likelihood and shortcut coalescence-based approaches, we analyze eight data sets, the largest of which contains 3,398 gene regions and 696,652 amino acid sites forming the largest phylogenomic analysis of spider relationships produced to date. Contrary to long held beliefs that the orb web is the crowning achievement of spider evolution, ancestral state reconstructions of web type support a phylogenetically ancient origin of the orb web, and diversification analyses show that the mostly ground-dwelling, web-less RTA clade diversified faster than orb weavers. Consistent with molecular dating estimates we report herein, this may reflect a major increase in biomass of non-flying insects during the Cretaceous Terrestrial Revolution 125–90 million years ago favoring diversification of spiders that feed on cursorial rather than flying prey. Our results also have major implications for our understanding of spider systematics. Phylogenomic analyses corroborate several well-accepted high level groupings: Opisthothele, Mygalomorphae, Atypoidina, Avicularoidea, Theraphosoidina, Araneomorphae, Entelegynae, Araneoidea, the RTA clade, Dionycha and the Lycosoidea. Alternatively, our results challenge the monophyly of Eresoidea, Orbiculariae, and Deinopoidea. The composition of the major paleocribellate and neocribellate clades, the basal divisions of Araneomorphae, appear to be falsified. Traditional Haplogynae is in need of revision, as our findings appear to support the newly conceived concept of Synspermiata. The sister pairing of filistatids with hypochilids implies that some peculiar features of each family may in fact be synapomorphic for the pair. Leptonetids now are seen as a possible sister group to the Entelegynae, illustrating possible intermediates in the evolution of the more complex entelegyne genitalic condition, spinning organs and respiratory organs.

In 1991, Robert S. Desowitz asked, “Did the primitive malaria begin as a parasite of some prehistoric reptile that later was picked up by a mosquito, or was it first a parasite of the mosquito that later became established in the reptile?” This question has been debated for years and is addressed in the present work in light of the fossil record of malarial organisms (Haemosporidia). The general consensus is that malaria evolved as a parasite of vertebrates (Manwell 1961, Desportes and Schrével 2013, Mattingly 1983); however, Huff (1945) felt that the malaria progenitor originated with the vector, and in their discussion of malaria evolution, Di Fiore et al. (2009) recognized that in the digenetic malarial life cycle, the vector is the definitive host and the vertebrate the intermediate host. This question has also been addressed with molecular data, but thus far, only very small DNA segments have been analyzed, resulting in incongruous and poorly resolved gene trees (Di Fiore et al. 2009). In the present analysis, fossils are used to determine the progenitors, ancient hosts, and original geographic provinces of malarial organisms.

Received 07 September 2015 Accepted 17 February 2016 Published 29 March 2016

Abstract

Suspension-feeding fishes such as goldfish and whale sharks retain prey without clogging their oral filters, whereas clogging is a major expense in industrial crossflow filtration of beer, dairy foods and biotechnology products. Fishes’ abilities to retain particles that are smaller than the pore size of the gill-raker filter, including extraction of particles despite large holes in the filter, also remain unexplained. Here we show that unexplored combinations of engineering structures (backward-facing steps forming d-type ribs on the porous surface of a cone) cause fluid dynamic phenomena distinct from current biological and industrial filter operations. This vortical cross-step filtration model prevents clogging and explains the transport of tiny concentrated particles to the oesophagus using a hydrodynamic tongue. Mass transfer caused by vortices along d-type ribs in crossflow is applicable to filter-feeding duck beak lamellae and whale baleen plates, as well as the fluid mechanics of ventilation at fish gill filaments.

The spliceosome is an RNA and protein molecular machine that cuts out introns from messenger RNAs. Agafonov et al. used cryo-electron microscopy to determine the structure of the largest intermediate subcomplex on the assembly pathway for the human spliceosome (see the Perspective by Cate). The structure shows substantial differences from the equivalent yeast complex. It also reveals how the subcomplex must dock onto the rest of the spliceosome and hints at the structural changes the complex must go through to form the mature spliceosome.

The U4/U6.U5 triple small nuclear ribonucleoprotein (tri-snRNP) is a major spliceosome building block. We obtained a three-dimensional structure of the 1.8-megadalton human tri-snRNP at a resolution of 7 angstroms using single-particle cryo–electron microscopy (cryo-EM). We fit all known high-resolution structures of tri-snRNP components into the EM density map and validated them by protein cross-linking. Our model reveals how the spatial organization of Brr2 RNA helicase prevents premature U4/U6 RNA unwinding in isolated human tri-snRNPs and how the ubiquitin C-terminal hydrolase–like protein Sad1 likely tethers the helicase Brr2 to its preactivation position. Comparison of our model with cryo-EM three-dimensional structures of the Saccharomyces cerevisiae tri-snRNP and Schizosaccharomyces pombe spliceosome indicates that Brr2 undergoes a marked conformational change during spliceosome activation, and that the scaffolding protein Prp8 is also rearranged to accommodate the spliceosome’s catalytic RNA network.

Look at a protein-coding gene in the genome of any eukaryote—be it animal, plant, fungus, or protist—and you will likely find the coding region fragmented by intervening sequences known as introns. When the gene is transcribed, these introns have to be removed from the pre-messenger RNA (pre-mRNA) before a protein can be made. How these introns are removed has been studied intensively for decades without the aid of a three-dimensional map of the highly dynamic machine at the heart of the process: the spliceosome. On page 1416 of this issue, Agafonov et al. report the first molecular-resolution reconstruction of a central assembly of the human spliceosome, the U4/U6.U5 triple small nuclear ribonucleoprotein (tri-snRNP) complex, using cryo-electron microscopy (cryo-EM) (1). Together with high-resolution cryo-EM reconstructions of spliceosome assemblies from fungi (2-5) and the x-ray crystal structure of the U1 snRNP (6), these structural models of the splicing machinery launch a new era in understanding eukaryotic gene regulation.

Lungfish and coelacanths are the only living sarcopterygian fish. The phylogenetic relationship of lungfish to the last common ancestor of tetrapods and their close morphological similarity to their fossil ancestors make this species uniquely interesting. However their genome size, the largest among vertebrates, is hampering the generation of a whole genome sequence. To provide a partial solution to the problem, a high-coverage lungfish reference transcriptome was generated and assembled. The present findings indicate that lungfish, not coelacanths, are the closest relatives to land-adapted vertebrates. Whereas protein-coding genes evolve at a very slow rate, possibly reflecting a “living fossil” status, transposable elements appear to be active and show high diversity, suggesting a role for them in the remarkable expansion of the lungfish genome. Analyses of single genes and gene families documented changes connected to the water to land transition and demonstrated the value of the lungfish reference transcriptome for comparative studies of vertebrate evolution.

A goal in biology is to understand the molecular and biological function of every gene in a cell. One way to approach this is to build a minimal genome that includes only the genes essential for life. In 2010, a 1079-kb genome based on the genome of Mycoplasma mycoides (JCV-syn1.0) was chemically synthesized and supported cell growth when transplanted into cytoplasm. Hutchison III et al. used a design, build, and test cycle to reduce this genome to 531 kb (473 genes). The resulting JCV-syn3.0 retains genes involved in key processes such as transcription and translation, but also contains 149 genes of unknown function.

Science, this issue p. 10.1126/science.aad6253

Structured Abstract

INTRODUCTION

In 1984, the simplest cells capable of autonomous growth, the mycoplasmas, were proposed as models for understanding the basic principles of life. In 1995, we reported the first complete cellular genome sequences (Haemophilus influenza, 1815 genes, and Mycoplasma genitalium, 525 genes). Comparison of these sequences revealed a conserved core of about 250 essential genes, much smaller than either genome. In 1999, we introduced the method of global transposon mutagenesis and experimentally demonstrated that M. genitalium contains many genes that are nonessential for growth in the laboratory, even though it has the smallest genome known for an autonomously replicating cell found in nature. This implied that it should be possible to produce a minimal cell that is simpler than any natural one. Whole genomes can now be built from chemically synthesized oligonucleotides and brought to life by installation into a receptive cellular environment. We have applied whole-genome design and synthesis to the problem of minimizing a cellular genome.

RATIONALE

Since the first genome sequences, there has been much work in many bacterial models to identify nonessential genes and define core sets of conserved genetic functions, using the methods of comparative genomics. Often, more than one gene product can perform a particular essential function. In such cases, neither gene will be essential, and neither will necessarily be conserved. Consequently, these approaches cannot, by themselves, identify a set of genes that is sufficient to constitute a viable genome. We set out to define a minimal cellular genome experimentally by designing and building one, then testing it for viability. Our goal is a cell so simple that we can determine the molecular and biological function of every gene.

RESULTS

Whole-genome design and synthesis were used to minimize the 1079–kilobase pair (kbp) synthetic genome of M. mycoides JCVI-syn1.0. An initial design, based on collective knowledge of molecular biology in combination with limited transposon mutagenesis data, failed to produce a viable cell. Improved transposon mutagenesis methods revealed a class of quasi-essential genes that are needed for robust growth, explaining the failure of our initial design. Three more cycles of design, synthesis, and testing, with retention of quasi-essential genes, produced JCVI-syn3.0 (531 kbp, 473 genes). Its genome is smaller than that of any autonomously replicating cell found in nature. JCVI-syn3.0 has a doubling time of ~180 min, produces colonies that are morphologically similar to those of JCVI-syn1.0, and appears to be polymorphic when examined microscopically.

CONCLUSION

The minimal cell concept appears simple at first glance but becomes more complex upon close inspection. In addition to essential and nonessential genes, there are many quasi-essential genes, which are not absolutely critical for viability but are nevertheless required for robust growth. Consequently, during the process of genome minimization, there is a trade-off between genome size and growth rate. JCVI-syn3.0 is a working approximation of a minimal cellular genome, a compromise between small genome size and a workable growth rate for an experimental organism. It retains almost all the genes that are involved in the synthesis and processing of macromolecules. Unexpectedly, it also contains 149 genes with unknown biological functions, suggesting the presence of undiscovered functions that are essential for life. JCVI-syn3.0 is a versatile platform for investigating the core functions of life and for exploring whole-genome design.

...

Abstract

We used whole-genome design and complete chemical synthesis to minimize the 1079–kilobase pair synthetic genome of Mycoplasma mycoides JCVI-syn1.0. An initial design, based on collective knowledge of molecular biology combined with limited transposon mutagenesis data, failed to produce a viable cell. Improved transposon mutagenesis methods revealed a class of quasi-essential genes that are needed for robust growth, explaining the failure of our initial design. Three cycles of design, synthesis, and testing, with retention of quasi-essential genes, produced JCVI-syn3.0 (531 kilobase pairs, 473 genes), which has a genome smaller than that of any autonomously replicating cell found in nature. JCVI-syn3.0 retains almost all genes involved in the synthesis and processing of macromolecules. Unexpectedly, it also contains 149 genes with unknown biological functions. JCVI-syn3.0 is a versatile platform for investigating the core functions of life and for exploring whole-genome design.

Fishes have adapted a number of different behaviors to move out of the water, but none have been described as being able to walk on land with a tetrapod-like gait. Here we show that the blind cavefish Cryptotora thamicola walks and climbs waterfalls with a salamander-like diagonal-couplets lateral sequence gait and has evolved a robust pelvic girdle that shares morphological features associated with terrestrial vertebrates. In all other fishes, the pelvic bones are suspended in a muscular sling or loosely attached to the pectoral girdle anteriorly. In contrast, the pelvic girdle of Cryptotora is a large, broad puboischiadic plate that is joined to the iliac process of a hypertrophied sacral rib; fusion of these bones in tetrapods creates an acetabulum. The vertebral column in the sacral area has large anterior and posterior zygapophyses, transverse processes, and broad neural spines, all of which are associated with terrestrial organisms. The diagonal-couplet lateral sequence gait was accomplished by rotation of the pectoral and pelvic girdles creating a standing wave of the axial body. These findings are significant because they represent the first example of behavioural and morphological adaptation in an extant fish that converges on the tetrapodal walking behaviour and morphology.

Preservation of soft-bodied organisms is exceedingly rare in the fossil record.One way that such fossils are preserved is as carbonaceous compressions in fined-grained marine sedimentary rocks. These deposits of exceptional preservation are known as Burgess Shale-type (BST) deposits. During the Cambrian Period, BST deposits are more common and provide a crucial view of early animal evolution. The earliest definitive fossil evidence for macroscopic animal-grade organisms is found in the preceding Ediacaran Period. BST deposits from the Ediacaran are rarer and lack conclusive evidence for animals. Here we report the discovery of a new Ediacaran BST deposit with exceptional preservation of non-mineralizing macro-organisms in thinly bedded black shale from Zavkhan Province, western Mongolia. This fossil assemblage, here named the Zuun-Arts biota, currently consists of two new species of probable macroscopic multicellular benthic algae. One species, Chinggiskhaania bifurcata n. gen., n. sp., dominates the biota. The other species, Zuunartsphyton delicatum n. gen., n. sp., is known from three specimens. SEM-EDS analysis shows that the fossils are composed of aluminosilicate clay minerals and some carbon, a composition comparable to fossils from the Cambrian Burgess Shale biota. This discovery opens a new window through which to view late Precambrian life.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

Cite this article

Otero RA. (2016) Taxonomic reassessment of Hydralmosaurus as Styxosaurus: new insights on the elasmosaurid neck evolution throughout the Cretaceous. PeerJ 4:e1777 https://doi.org/10.7717/peerj.1777

Two extremely-long necked elasmosaurids, AMNH 1495, holotype of Hydralmosaurus serpentinus, and AMNH 5835, previously referred to H. serpentinus, are here reviewed in detail. Unique features of the cervical vertebrae, which are only present on elasmosaurids from the Western Interior Seaway, are recognized based on these specimens and by comparison with penecontemporaneous taxa with biogeographic affinities. Phylogenetic analysis, bivariate graphic analysis of cervical vertebrae proportions, comparisons of different cervical vertebral types, paleobiogeographic distribution and study of the elasmosaurid axial evolution throughout the Cretaceous are here integrated. As a result, at least two separate lineages within the Elasmosauridae are identified by independently acquired extremely-long necks (over 60 cervical vertebrae). First, a still scarcely known lineage is so far represented by the lower Cenomanian Thalassomedon haningtoni, the Turonian Libonectes morgani and close relatives. A second lineage is here defined as a new clade, the Styxosaurinae, which groups the Campanian genera Terminonatator, Styxosaurus (=‘Hydralmosaurus’), Albertonectes and Elasmosaurus, the two latter forming a derived branch that includes the most extreme amniote necks known to date (more than 70 cervical vertebrae). Phylogenetic analysis supports AMNH 1495 and AMNH 5835 as being closely related to Styxosaurus snowii. Therefore, the species Styxosaurus browni is re-validated, while AMNH 1495 is here referred to Styxosaurus sp. This research also recognizes the ‘Cimoliasauridae’ (nomen dubium) as a paraphyletic group but informative of a plesiomorphic cervical vertebral morphology of elasmosaurids which was persistent throughout the whole Cretaceous and from whom aristonectines, styxosaurines and Thalassomedon and close relatives are derived. The genus Hydralmosaurus is recommended for being abandoned.

Cite this as Otero RA. (2016) Taxonomic reassessment of Hydralmosaurus as Styxosaurus: new insights on the elasmosaurid neck evolution throughout the Cretaceous. PeerJ 4:e1777 https://doi.org/10.7717/peerj.1777

The nuclear pore complex (NPC) is responsible for nucleocytoplasmic transport and constitutes a hub for control of gene expression. The components of NPCs from several eukaryotic lineages have been determined, but only the yeast and vertebrate NPCs have been extensively characterized at the quaternary level. Significantly, recent evidence indicates that compositional similarity does not necessarily correspond to homologous architecture between NPCs from different taxa. To address this, we describe the interactome of the trypanosome NPC, a representative, highly divergent eukaryote. We identify numerous new NPC components and report an exhaustive interactome, allowing assignment of trypanosome nucleoporins to discrete NPC substructures. Remarkably, despite retaining similar protein composition, there are exceptional architectural dissimilarities between opisthokont (yeast and vertebrates) and excavate (trypanosomes) NPCs. Whilst elements of the inner core are conserved, numerous peripheral structures are highly divergent, perhaps reflecting requirements to interface with divergent nuclear and cytoplasmic functions. Moreover, the trypanosome NPC has almost complete nucleocytoplasmic symmetry, in contrast to the opisthokont NPC; this may reflect divergence in RNA export processes at the NPC cytoplasmic face, as we find evidence supporting Ran-dependent mRNA export in trypanosomes, similar to protein transport. We propose a model of stepwise acquisition of nucleocytoplasmic mechanistic complexity and demonstrate that detailed dissection of macromolecular complexes provides fuller understanding of evolutionary processes.

Author Summary

Much of the core architecture of the eukaryotic cell was established over one billion years ago. Significantly, many cellular systems possess lineage-specific features, and architectural and compositional variation of complexes and pathways that are likely keyed to specific functional adaptations. The nuclear pore complex (NPC) contributes to many processes, including nucleocytoplasmic transport, interactions with the nuclear lamina, and mRNA processing. We exploited trypanosome parasites to investigate NPC evolution and conservation at the level of protein–protein interactions and composition. We unambiguously assigned NPC components to specific substructures and found that the NPC structural scaffold is generally conserved, albeit with lineage-specific elements. However, there is significant variation in pore membrane proteins and an absence of critical components involved in mRNA export in fungi and animals (opisthokonts). This is reflected by the completely symmetric localization of all trypanosome nucleoporins, with the exception of the nuclear basket. This architecture is highly distinct from opisthokonts. We also identify features that suggest a Ran-dependent system for mRNA export in trypanosomes, a system that may presage distinct mechanisms of protein and mRNA transport in animals and fungi. Our study highlights that shared composition of macromolecular assemblies does not necessarily equate to shared architecture. Identification of lineage-specific features within the trypanosome NPC significantly advances our understanding of mechanisms of nuclear transport, gene expression, and evolution of the nucleus.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: This work is supported in whole or part by The National Institutes of Health grants: NIAID Exploratory/Developmental Research Grant 1R21AI096069 (to MPR), NIGMS GM103314 (to BTC), GM103511 and GM109824 (to MPR and BTC); and Wellcome Trust grant 082813/Z/07/Z (to MCF and MPR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

sábado, março 19, 2016

Limits of time in cosmology

Abstract

We provide a discussion of some main ideas in our project about the physical foundation of the time concept in cosmology. It is standard to point to the Planck scale (located at $\sim 10^{-43}$ seconds after a fictitious "Big Bang" point) as a limit for how far back we may extrapolate the standard cosmological model. In our work we have suggested that there are several other (physically motivated) interesting limits -- located at least thirty orders of magnitude before the Planck time -- where the physical basis of the cosmological model and its time concept is progressively weakened. Some of these limits are connected to phase transitions in the early universe which gradually undermine the notion of 'standard clocks' widely employed in cosmology. Such considerations lead to a 'scale problem' for time which becomes particularly acute above the electroweak phase transition (before $\sim 10^{-11}$ seconds). Other limits are due to problems of building up a cosmological reference frame, or even contemplating a sensible notion of proper time, if the early universe constituents become too quantum. This 'quantum problem' for time arises e.g. if a pure quantum phase is contemplated at the beginning of inflation at, say, $\sim 10^{-34}$ seconds.

It is a plain fact that biology makes use of terms and expressions commonly spoken of as teleological. Biologists frequently speak of the function of biological items.They may also say that traits are 'supposed to' perform some of their effects, claim that traits are 'for' specific effects, or that organisms have particular traits 'in order to' engage in specific interactions.There is general agreement that there must be something useful about this linguistic practice but it is controversial whether it is entirely appropriate, and if so why it is.

Many theorists have defended the use of seemingly teleological terms by appeal to an etiological notion of function (Wright, 1973; Millikan, 1984, 2002; Neander, 1991; Griffiths, 1993; Godfrey-Smith, 1994; and Buller, 1999). According to the etiological notion, attributing a function to a trait is a matter of pointing to effects that account for why the trait has been selected for. On an alternative but related formulation function statements indicate that past tokens of the targeted type contributed to the existence of current token traits in virtue of exhibiting the effect at issue. A central feature of etiological definitions is that they come with a requirement of ancestry; there must have been type-identical tokens exhibiting the targeted effect in order for a trait to have an etiological function. Trivially, first-generation tokens lack such ancestors as far as the novel trait is concerned and therefore lack etiological functions.

In this paper, I will home in on the theoretical motivation for the requirement of ancestry, a requirement that renders the resulting functions essentially etiological. I will argue that the positing of etiological functions is theoretically ungrounded. Not that there aren't any tokens that meet the description, but this is far from sufficient. So, for instance, there is a real difference between tokens with a trait T that are born 2000 years or more after the first token with T, and tokens that are born earlier. We may then add to a standard etiological definition of 'function' the requirement of being born 2000 years or more after the first mutant and let 'munction' stand for the resulting historical property. Are there munctions? Well, if all that is required in order to answer affirmatively is that there are tokens that fit the description then the answer is clearly 'yes.' However, there is no known reason for stressing that particular difference and therefore no reason to posit munctions. Likewise, the point of this paper is that there is no theoretical reason to stress the difference between first-generation tokens and later ones and thus no reason to conceive of biological functions as essentially etiological.

There is nothing new about voicing negative verdicts about etiological accounts of 'function' (Cummins, 1975, 2002; Enç and Adams, 1992; Walsh and Ariew, 1996; Davies, 2000a, b; McLaughlin, 2001; Lewens, 2004). I take my approach to differ from, and be a useful complement to, that of others in the following respects: I press the question of the rationale for the exclusion, by definition, of first-generation tokens more consistently than has been done elsewhere. I attempt to run through the main considerations etiologists have brought to bear on the topic. In the process I look into the claim that the etiological notion of function is required for biological categorisation, and critically address relatively recent proposals made by etiologists on this issue. I look at Millikan's (1984) explicit motivation for her 'proper function' — that it is required to capture explanatory analogies between domains — and find that this motivation fails to suggest an etiological notion as opposed to a non-etiological one. I provide a rather thorough critical discussion of the idea, made popular by Wright (1973), that the etiological notion is vindicated by its role in explaining the existence of traits. I also discuss the possibility of finding support for the etiological account in the writings of prominent biologists and conclude that the textual evidence is not unequivocally in favour of an etiological account. All things considered, I take my account to strongly suggest that the etiological account of functions gets its support from a pre-theoretical mindset, not theoretical considerations.